York began his working days as a financial analyst for Guggenheim Partners at their New York City offices but left after approximately a year.[1] After he quit his first job, York's parents brought him into their family owned team, the San Francisco 49ers, as the Director of Strategic Planning[1] and later promoted their son to Vice President of Strategic Planning.[3]

On December 28, 2008 Jed was appointed by his father to become president of the 49ers. While Jed is the operating head of the franchise, his mother Denise is the principal owner, and both of his parents, as co-chairmen, are responsible for providing resources and maintain their role of interacting with other owners and NFL executives.[4]

On October 11, 2010, with the 49ers off to a disappointing 0-5 start, Jed York wrote to ESPN's Adam Schefter that the 49ers would win their division and make the playoffs.[5] This proclamation led ESPN columnist David Fleming to refer to York as "kooky" and "goofy" and to note that York "backs up such bold declarations with a long list of qualifications starting with (1) his lifelong love of the 49ers, (2) his prestigious high school baseball career and (3) the fact that his godfather is Eddie DeBartolo."[6] However, the 49ers did come within one game of backing up York's assertion. In 2011, the Niners finished the season 13-3 with the 2nd seed in the NFC. In the divisional round, the Niners defeated the New Orleans Saints. York's 49ers then hosted the NFC Championship game against the New York Giants, eventually losing in overtime, 20-17. The success of the 2011 San Francisco 49ers was accomplished with much of the same team from 2010, but with the key addition of first-year head coach Jim Harbaugh.

In 2012, Jed York was replaced by Gideon Yu as Team President, although he retained the title of CEO.[7]

After a disappointing 19-3 loss to divisional rival Seattle Seahawks on November 27, 2014, York tweeted “Thank you 49ers faithful for coming out strong tonight. This performance wasn’t acceptable. I apologize for that.”[8] This public statement sparked a media frenzy about York's intent behind the Tweet and whether he was specifically referring to Coach Jim Harbaugh's future, prompting Lowell Cohn, a columnist with the The Press Democrat, to declare: "Jed York is a coward."[9]

After the controversial decision to fire head coach Jim Harbaugh, there was a large negative outcry from the media and the 49ers fan base. Commenting on York's ability to manage the critical relationship between the general manager and the head coach, Michael Rosenberg wrote in Sports Illustrated, "he failed completely."[10] Rosenberg also described York's impact on the broader 49ers organization, noting that "York has created a culture that encourages selfishness, weakness and back-stabbing." Throughout the season, there were numerous leaks to the media from within the 49ers organization criticizing Coach Harbaugh. San Jose Mercury News columnist Tim Kawakami noted "York and [General Manager, Trent] Baalke were the primary sources for the off-the-record disclosures that undercut Harbaugh’s tenure."[11]